Ecological relevance of flagellar motility in soil bacterial communities

Josep Ramoneda; Kunkun Fan; Jane M Lucas; Haiyan Chu; Andrew Bissett; Michael S Strickland; Noah Fierer

doi:10.1093/ismejo/wrae067

Ecological relevance of flagellar motility in soil bacterial communities

ISME J. 2024 Apr 22:wrae067. doi: 10.1093/ismejo/wrae067. Online ahead of print.

Authors

Josep Ramoneda^{1

2}, Kunkun Fan³, Jane M Lucas⁴, Haiyan Chu^{3

5}, Andrew Bissett⁶, Michael S Strickland⁷, Noah Fierer^{1

8}

Affiliations

¹ Cooperative Institute for Research in Environmental Sciences (CIRES), University of Colorado, Boulder, Colorado, United States.
² Spanish Research Council (CSIC), Center for Advanced Studies of Blanes (CEAB), Blanes, Spain.
³ Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, China.
⁴ Cary Institute of Ecosystem Studies, Millbrook, New York, United States.
⁵ University of Chinese Academy of Sciences, Beijing, China.
⁶ CSIRO, Hobart, TAS7000, Australia.
⁷ Department of Soil and Water Systems, University of Idaho, Moscow, Idaho, United States.
⁸ Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, United States.

PMID: 38648266
DOI: 10.1093/ismejo/wrae067

Abstract

Flagellar motility is a key bacterial trait as it allows bacteria to navigate their immediate surroundings. Not all bacteria are capable of flagellar motility, and the distribution of this trait, its ecological associations, and the life history strategies of flagellated taxa remain poorly characterized. We developed and validated a genome-based approach to infer the potential for flagellar motility across 12 bacterial phyla (26 192 genomes in total). The capacity for flagellar motility was associated with a higher prevalence of genes for carbohydrate metabolism and higher maximum potential growth rates, suggesting that flagellar motility is more prevalent in environments with higher carbon availability. To test this hypothesis, we applied a method to infer the prevalence of flagellar motility in whole bacterial communities from metagenomic data, and quantified the prevalence of flagellar motility across 4 independent field studies that each captured putative gradients in soil carbon availability (148 metagenomes). As expected, we observed a positive relationship between the prevalence of bacterial flagellar motility and soil carbon availability in all datasets. Since soil carbon availability is often correlated with other factors that could influence the prevalence of flagellar motility, we validated these observations using metagenomic data acquired from a soil incubation experiment where carbon availability was directly manipulated with glucose amendments. This confirmed that the prevalence of bacterial flagellar motility is consistently associated with soil carbon availability over other potential confounding factors. This work highlights the value of combining predictive genomic and metagenomic approaches to expand our understanding of microbial phenotypic traits and reveal their general environmental associations.

Keywords: community-aggregated traits; flagellar motility; machine learning; microbial life history strategies; soil bacterial community; soil carbon; trait-based microbial ecology.